Five tropical air-breathing fishes, six different strategies to defend against ammonia toxicity on land

Physiological and Biochemical Zoology

Volumn 77, Issue 5, 2004, Pages 768-782

  Ip, Y K ^a   Chew, S F ^b   Randall, D J ^c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMMONIA; NITROGEN; UREA;

AMMONIA; FISH; RESPIRATION;

ADAPTATION; ANIMAL; COMPARATIVE STUDY; CONFERENCE PAPER; ENVIRONMENT; FISH; METABOLISM; OXYGEN CONSUMPTION; PHYSIOLOGY; SPECIES DIFFERENCE; TROPIC CLIMATE;

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS; AMMONIA; ANIMALS; ENVIRONMENT; FISHES; NITROGEN; OXYGEN CONSUMPTION; SPECIES SPECIFICITY; TROPICAL CLIMATE; UREA;

BOSTRYCHUS SINENSIS; CHANNA; CHANNA ASIATICA; CHELONE GLABRA; MISGURNUS; MISGURNUS ANGUILLICAUDATUS; PERIOPHTHALMUS BARBARUS; PISCES; PROTOPTERUS AETHIOPICUS; PROTOPTERUS DOLLOI;

EID: 6344238909     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/422057     Document Type: Conference Paper

References (124)

1. Anderson P.M. 2001. Urea and glutamine synthesis: environmental influences on nitrogen excretion. Pp. 239-277 in P.A. Wright and P.M. Anderson, eds. Fish Physiology. Vol. 20. Nitrogen Excretion. Academic Press, New York.
2. Anderson P.M., M.A. Broderius, K.C. Fong, T.K.N. Tsui, S.F. Chew, and Y.K. Ip. 2002. Glutamine synthetase expression in liver, muscle, stomach and intestine of Bostrichyths sinensis in response to exposure to a high exogenous ammonia concentration. J Exp Biol 205:2053-2065.
3. Arillo A., C. Margiocco, F. Melodia, P. Mensi, and G. Schenone. 1981. Ammonia toxicity mechanisms in fish: studies on rainbow trout (Salmo gairdneri Rich). Ecotoxicol Environ Saf 5:316-325.
4. Benton M.J. 1990. Phylogeny of the major tetrapod groups: morphological data and divergence dates. J Mol Evol 30:409-424.
5. Binstock L. and H. Lecar. 1969. Ammonium ion currents in the squid giant axon. J Gen Physiol 53:342-361.
6. Blei A.T., S.M. Olafsson, G. Therrien, and R.F. Butterworth. 1994. Ammonia-induced cerebral edema and intracranial hypertension in rats after portacaval anastomosis. Hepatology 19:1431-1444.
7. Bradford H.F., H.K. Ward, and P. Foley. 1989. Glutaminase inhibition and release of neurotransmitter glutamate from synaptosomes. Brain Res 476:29-34.
8. Brusilow S.W. 2002. Hyperammoniemic encephalopathy. Medicine 81:240-249.
9. Campbell J.W. 1973. Excretory nitrogen metabolism. Pp. 279-316 in C.L. Prosser, ed. Comparative Animal Physiology. 3d ed. Saunders, Philadelphia.
10. _. 1991. Excretory nitrogen metabolism. Pp. 277-324 in C. L. Prosser, ed. Comparative Animal Physiology. Vol. 1. Environmental and Metabolic Animal Physiology. 4th ed. Wiley, New York.
11. Campbell J.W. and P.M. Anderson. 1991. Evolution of mitochondrial enzyme systems in fish: the mitochondrial synthesis of glutamine and citrulline. Pp. 43-75 in P.W. Hochachka and T.P. Mommsen, eds. Biochemistry and Molecular Biology of Fishes. Vol. 1. Phylogenetic and Biochemical Perspectives. Elsevier, Amsterdam.
12. Campbell J.W. and J.E. Vorhaben. 1983. Mitochondrial ammoniagenesis in liver of the channel catfish Ictalurus punctatus. Am J Physiol 244:R709-R717.
13. Chew S.F., N.K.Y. Chan, W.L. Tam, A.M. Loong, K.C. Hiong, and Y.K. Ip. 2004. Nitrogen metabolism in the African lungfish (Protopterus dolloi) aestivating in a mucus cocoon on land. J Exp Biol 207:777-786.
14. Chew S.F., E.Y.L. Goh, C.B. Lim, and Y.K. Ip. 1998. Cyanide exposure affected the production and excretion of ammonia in the mudskipper Boleophthalmus boddaerti. Comp Biochem Physiol 120C:441-448.
15. Chew S.F. and Y.K. Ip. 1990. Differences in the responses of two mudskippers, Boleophthalmus boddaerti and Periophthalmus chrysospilos, to changes in salinity. J Exp Zool 256:227-231.
16. _. 1992a. Biochemical adaptations of the mudskipper, Boleophthalmus boddaerti, to a lack of oxygen. Mar Biol 112:567-572.
17. _. 1992b. Cyanide detoxification in the mudskipper, Boleophthalmus boddaerti. J Exp Zool 261:1-9.
18. _. 1992c. Tolerance of the mudskipper Boleophthalmus boddaerti to a lack of oxygen. Zool Sci 9:227-230.
19. Chew S.F., Y. Jin, and Y.K. Ip. 2001. The loach Misgurnus anguillicaudatus reduces amino acid catabolism and accumulates alanine and glutamine during aerial exposure. Physiol Biochem Zool 74:226-237.
20. Chew S.F., A.L.L. Lim, W.P. Low, G.L. Lee, K.M. Chan, and Y.K. Ip. 1990. Can the mudskipper, Periophthalmus chrysospilos, tolerate acute environmental hypoxic exposure? Fish Physiol Biochem 8:221-227.
21. Chew S.F., T.F. Ong, L. Ho, W.L. Tam, A.M. Loong, K.C. Hiong, W.P. Wong, and Y.K. Ip. 2003a. Urea synthesis in the African lungfish Protopterus dolloi - hepatic carbamoyl phosphate synthetase III and glutamine synthetase can be up-regulated by 6 days of aerial exposure. J Exp Biol 206:3615-3624.
22. Chew S.F., J.M. Wilson, Y.K. Ip, and D.J. Randall. In press. Nitrogenous excretion and defense against ammonia toxicity. In A.L. Val, V.M. Almedia-Val, and D.J. Randall, eds. Fish Physiology. Vol. 23. The Physiology of Tropical Fishes. Academic Press, New York.
23. Chew S.F., M.Y. Wong, W.L. Tam, and Y.K. Ip. 2003b. The snakehead Channa asiatica accumulates alanine during aerial exposure, but is incapable of sustaining locomotory activities on land through partial amino acid catabolism. J Exp Biol 206:693-704.
24. Cooper J.L. and F. Plum. 1987. Biochemistry and physiology of brain ammonia. Physiol Rev 67:440-519.
25. Davenport J. and M.D.J. Sayer. 1986. Ammonia and urea excretion in the amphibious teleost Blennius pholis (L.) in seawater and in air. Comp Biochem Physiol A 84:189-194.
26. Eddy F.B., O.S. Bamford, and G.M.O. Maloiy. 1980. Sodium and chloride balance in the African catfish Clarias mossambicus. Comp Biochem Physiol A 66:637-641.
27. Fan P. and J.C. Szerb. 1993. Effects of ammonium ions on synaptic transmission and on responses to quisqualate and N-methyl-D-aspartate in hippocampal CA1 pyramidal neurons in vitro. Brain Res 632:225-231.
28. Felipo V. and R.F. Butterworth. 2002. Neurobiology of ammonia. Prog Neurobiol 67:259-279.
29. Felipo V., E. Kosenko, M.D. Minana, G. Marcaida, and S. Grisolia. 1994. Molecular mechanism of acute ammonia toxicity and of its prevention by L-carnitine. Pp. 65-77 in V. Felipo and S. Grisola, eds. Hepatic Encephalopathy, Hyperammonemia and Ammonia Toxicity. Plenum, New York.
30. Frick N.T. and P.A. Wright. 2002. Nitrogen metabolism and excretion in the mangrove killifish Rivulus marmoratus. II. Significant ammonia volatilization in a teleost during air-exposure. J Exp Biol 205:91-100.
31. Fromm P.O. and J.R. Gillette. 1968. Effects of ambient ammonia on blood ammonia and nitrogen excretion of rainbow trout (Salmo gairdneri). Comp Biochem Physiol 26:887-896.
32. Gilles R. and A. Pequeux. 1981. Cell volume regulation in crustaceans: relationship between mechanisms for controlling the osmolaity of extracellular and intracellular fluids. J Exp Zool 215:351-362.
33. Gordon M.S. 1970. Patterns of nitrogen excretion in amphibious fishes. J Exp Biol 53:559-572.
34. Gordon M.S., I. Boetius, D.H. Evans, R. McCarthy, and L.C. Oglesby. 1969. Aspects of the physiology of terrestrial life in amphibious fishes. I. The mudskipper, Periophthalmus sobrinus. J Exp Biol 50:141-149.
35. Gordon M.S., I. Boetius, D.H. Evans, and L.C. Oglesby. 1968. Additional observations on the natural history of the mudskipper fish. Copeia 1968:853-857.
36. Gordon M.S., S. Fischer, and E. Tarifeno. 1970. Aspects of the physiology of terrestrial life in amphibious fishes. II. The Chilean clingfish, Sicyases sanguineus. J Exp Biol 53:559-572.
37. Gordon M.S., W.W.M. Ng, and A.Y.W. Yip. 1978. Aspects of the physiology of terrestrial life in amphibious fishes. III. The Chinese mudskipper Periophthalmus cantonensis. J Exp Biol 72:57-75.
38. Graham J.B. 1997. Air-Breathing Fishes: Evolution, Diversity, and Adaptation. Academic Press, San Diego, Calif.
39. Greenaway P. 1991. Nitrogenous excretion in aquatic and terrestrial crustaceans. Mem Queensl Mus 31:215-227.
40. Gregory R.B. 1977. Synthesis and total excretions of waste nitrogen by fish of the Periophthalmus (mudskipper) and Scartelaos families. Comp Biochem Physiol A 57:33-36.
41. Hansson E., F. Blomstrand, S. Khabiti, T. Olsson, and L. Ronnback. 1997. Glutamate induced astroglial swelling - methods and mechanisms. Acta Neurochir 70:148-151.
42. Hermenegildo C., G. Marcaida, C. Montoliu, S. Grisolia, M. Minana, and V. Felipo. 1996. NMDA receptor antagonists prevent acute ammonia toxicity in mice. Neurochem Res 21:1237-1244.
43. Hermenegildo C., C.P. Monfor, and V. Felipo. 2000. Activation of N-methyl-D-aspartate receptors in rat brain in vivo following acute ammonia intoxication: characterization by in vivo brain microdialysis. Hepatology 31:709-715.
44. Hilgier W., M. Zielińska, H.D. Borkowska, R. Gadamski, M. Walski, S.S. Oja, P. Saransaari, and J. Albrecht. 1999. Changes in the extracellular profiles of neuroactive amino acids in the rat striatum at the symptomatic stage of hepatic failure. J Neurosci Res 56:76-84.
45. Hillaby B.A. and D.J. Randall. 1979. Acute ammonia toxicity and ammonia excretion in rainbow trout (Salmo gairdneri). J Fish Res Board Can 36:621-629.
46. Ip Y.K., S.F. Chew, I.W.A. Leong, Y. Jin, and R.S.S. Wu. 2001a. The sleeper Bostrichthys sinensis (teleost) stores glutamine and reduces ammonia production during aerial exposure. J Comp Physiol B 171:357-367.
47. Ip Y.K., S.F. Chew, A.L.L. Lim, and W.P. Low. 1990. The mudskipper. Pp. 83-95 in L.M. Chou and P.K.L. Ng, eds. Essays in Zoology: Papers Commemorating the 40th Anniversary of the Department of Zoology. National University of Singapore Press, Singapore.
48. Ip Y.K., S.F. Chew, and D.J. Randall. 2001b. Ammonia toxicity, tolerance and excretion. Pp. 109-148 in P.A. Wright and P.M. Anderson, eds. Fish Physiology. Vol. 20. Nitrogen Excretion. Academic Press, New York.
49. Ip Y.K., S.F. Chew, J.M. Wilson, and D.J. Randall. 2004a. Defences against ammonia toxicity in tropical air-breathing fishes exposed to high concentrations of environmental ammonia: a review. J Comp Physiol B 174:565-575.
50. Ip Y.K., S.S.L. Kuah, and S.F. Chew. 2004b. Strategies adopted by the mudskipper, Boleophthalmus boddaerti, to survive sulfide exposure in normoxia or hypoxia. Physiol Biochem Zool 77:824-37.
51. Ip Y.K., C.Y. Lee, S.F. Chew, W.P. Low, and K.W. Peng. 1993. Differences in the responses of two mudskippers to terrestrial exposure. Zool Sci 10:511-519.
52. --ATPase activities to changes in salinity. Fish Physiol Biochem 9:63-68.
53. Ip Y.K., C.B. Lim, S.F. Chew, J.M. Wilson, and D.J. Randall. 2001c. Partial amino acid catabolism leading to the formation of alanine in Periophthalmodon schlosseri (mudskipper): a strategy that facilitates the use of amino acids as an energy source during locomotory activity on land. J Exp Biol 204:1615-1624.
54. 3 permeability in the skin. J Exp Biol 207:787-801.
55. Ip Y.K., R.M. Subaidah, P.C. Liew, A.M. Loong, K.C. Hiong, W.P. Wong, and S.F. Chew. 2004d. African sharptooth catfish Clarias gariepinus does not detoxify ammonia to urea or amino acids but actively excretes ammonia during exposure to environmental ammonia. Physiol Biochem Zool 77:242-254.
56. Iwata K., M. Kakuta, G. Ikeda, S. Kimoto, and N. Wada. 1981. Nitrogen metabolism in the mudskipper, Periophthalmus cantonensis: a role of free amino acids in detoxification of ammonia produced during its terrestrial life. Comp Biochem Physiol A 68:589-596.
57. Janssens P.A. and P.P. Cohen. 1966. Ornithine-urea cycle enzymes in the African lungfish, Protopterus aethiopicas. Science 152:358-359.
58. _. 1968a. Nitrogen metabolism in the African lungfish. Comp Biochem Physiol 24:879-886.
59. _. 1968b. Biosynthesis of urea in the estivating African lungfish and in Xenopus laevis under conditions of water shortage. Comp Biochem Physiol 24:887-898.
60. Jow L.Y., S.F. Chew, C.B. Lim, P.M. Anderson, and Y.K. Ip. 1999. The marble goby Oxyeleotris marmoratus activates hepatic glutamine synthetase and detoxifies ammonia to glutamine during air exposure. J Exp Biol 202:237-245.
61. Kimelberg H.K., S.K. Goderie, S. Higman, S. Pang, and R.A. Waniewski. 1990. Swelling-induced release of glutamate, aspartate and taurine from astrocyte culture. J Neurosci 10:1583-1591.
62. Kloppick E., G. Jacobasch, and S. Rapoport. 1967. Steigerung der glykolyse durch den einfluss von ammoniiumionen auf die phosphofruktokinaseaktivitat (Enhancement of the glycolytic rate by action of ammonium ion on phosphofructokinase activity). Acta Biol Med Ger 18:37-42.
63. Kok T.W.K., C.B. Lim, T.J. Lam, and Y.K. Ip. 1998. The mudskipper Periophthalmodon schlosseri respires more efficiently on land than in water and vice versa for Boleophthalmus boddaerti. J Exp Zool 280:86-90.
64. Kormanik G.A. and D.H. Evans. 1988. Nitrogenous waste excretion in the intertidal rock gunnel (Pholis gunnellus L.): the effects of emersion. Bull Mt Desert Isl Biol Lab 27:33-35.
65. Kosenko E., Y. Kaminsky, V. Felipo, M.D. Minana, and S. Grisolia. 1993. Chronic hyperammonemia prevents changes in brain energy and ammonia metabolites induced by acute ammonium intoxication. Biochim Biophys Acta 1180:321-326.
66. Kosenko E., Y. Kaminsky, E. Grau, M.D. Minana, S. Grisolia, and V. Felipo. 1995. Nitoarginine, an inhibitor of nitric oxide synthetase, attenuates ammonia toxicity and ammonia-induced alterations inbrain metabolism. Neurochem Res 20:451-456.
67. +-ATPase. J Neurochem 63:2172-2178.
68. Kosenko E., Y. Kaminsky, A. Kaminsky, M. Valencia, L. Lee, C. Hermenegildo, and V. Felipo. 1997. Superoxide production and antioxidant enzymes in ammonia intoxication in rats. Free Radic Res 27:637-644.
69. Kosenko E., Y. Kaminsky, O. Lopata, N. Muravyov, and V. Felipo. 1999. Blocking NMDA receptors prevents the oxidative stress induced by acute ammonia intoxication. Free Radiv Biol Med 26:1369-1374.
70. Kosenko E., Y. Kaminsky, I.G. Stavroskaya, and V. Felipo. 2000. Alteration of mitochondrial calcium homeostasis by ammonia-induced activation of NMDA receptors in rat brain in vivo. Brain Res 880:139-146.
71. Lim C.B., P.M. Anderson, S.F. Chew, and Y.K. Ip. 2001. Reduction in the rates of protein and amino acid catabolism to slow down the accumulation of endogenous ammonia: a strategy potentially adopted by mudskippers (Periophthalmodon schlosseri and Boleophthalmus boddaerti) during aerial exposure in constant darkness. J Exp Biol 204:1605-1614.
72. Livingstone D.R. 1985. Biochemical measurements. Pp. 81-132 in B.L. Bayne, D.A. Brown, K. Burns, D.R. Dixons, A. Ivanovici, D.R. Livingstone, D.M. Lowe, M.N. Moore, A.R.D. Stebbing, and J. Widdows, eds. The Effects of Stress and Pollution on Marine Animals. Praeger, New York.
73. Low W.P., D.J.W. Lane, and Y.K. Ip. 1988. A comparative study of terrestrial adaptations in three mudskippers - Periophthalmus chrysospilos, Boleophthalmus boddaerti and Periophthalmodon schlosseri. Biol Bull 175:434-438.
74. _. 1990. A comparative study of the gill morphometry in three mudskippers - Periophthalmus chrysospilos, Boleophthalmus boddaerti and Periophthalmus schlosseri. Zool Sci 7:29-38.
75. Marcaida G., V. Felipo, C. Hermenegildo, M.D. Minana, and S. Grisolia. 1992. Acute ammonia toxicity is mediated by NMDA type of glutamate receptors. Fed Eur Biochem Soc Lett 296:67-68.
76. Marcaida G., M.D. Minana, M. Burgal, S. Grisolia, and V. Felipo. 1995. Ammonia prevents activation of NMDA receptors by glutamate in rat cerebellar neuronal cultures. Eur J Neurosci 7:2389-2396.
77. 2 and ammonia on ventilation in trout. Fish Physiol Biochem 10:507-515.
78. McMahon B.R. and W.W. Burggren. 1987. Respiratory physiology of intestinal air breathing in the teleost fish Misgurnus anguillicaudatus. J Exp Biol 133:371-393.
79. Michalak A., C. Rose, J. Butterworth, and R.F. Butterworth. 1996. Neuroactive amino acids and glutamate (NMDA) receptors in frontal cortex of rats with experimental acute liver failure. Hepatology 24:908-914.
80. Mommsen T.P. and P.J. Walsh. 1989. Evolution of urea synthesis in vertebrates: the piscine connection. Science 243:72-75.
81. _. 1992. Biochemical and environmental perspectives on nitrogen metabolism in fishes. Experientia 48:583-593.
82. Morii H. 1979. Changes with time ammonia and urea concentrations in the blood and tissue of mudskipper fish Periophthalmus cantonensis and Boelophthalmus pectinirostris kept in water and on land. Comp Biochem Physiol A 64:235-243.
83. Morii H., K. Nishikata, and O. Tamura. 1978. Nitrogen excretion of mudskipper fish Periophthalmus cantonensis and Boleophthalmus pectinirostris in water and on land. Comp Biochem Physiol A 60:189-193.
84. _. 1979. Ammonia and urea excretion from mudskipper fishes Periophthalmus cantonensis and Boleophthalmus pectinirostris transferred from land to water. Comp Biochem Physiol A 63:23-28.
85. Murdy E.O. 1989. A taxonomic revision and cladistic analysis of the oxudercine gobies (Gobiidae: Oxudercinae). Rec Aust Mus Suppl 11:1-93.
86. Murray B.W., E.R. Busby, T.P. Mommsen, and P.A. Wright. 2003. Evolution of glutamine synthetase in vertebrates: multiply glutamine synthetase genes expressed in rainbow trout (Oncorhynchus mykiss). J Exp Biol 206:1511-1521.
87. Oppong K.N.W., K. Bartlett, C.O. Record, and H. Al Mardini. 1995. Synaptosomal glutamate transport in thioacetamide-induced hepatic encephalopathy. Hepatology 22:553-558.
88. Pasti L., M. Zonta, T. Pozzan, S. Vicini, and G. Carmignoto. 2001. Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. J Neurosci 21:477-484.
89. 3 concentration of 446 and 36 μM, respectively. Fish Physiol Biochem 19:59-69.
90. Person-Le Ruyet J., R. Galland, A. Le Roux, and H. Chartois. 1997. Chronic ammonia toxicity in juvenile turbot (Scophthalmus maximus). Aquaculture 154:155-171.
91. Ramaswamy M. and T.G. Reddy. 1983. Ammonia and urea excretion in three species of air-breathing fish subjected to aerial exposure. Proc Ind Acad Sci Anim Sci 92:293-297.
92. Randall D.J. and T.K.N. Tsui. 2002. Ammonia toxicity in fish. Mar Pollut Bull 45:17-23.
93. + against a concentration gradient. Am J Physiol 46:R1562-R1567.
94. Randall D.J., C.M. Wood, S.F. Perry, H. Bergman, G.M.O. Maloiy, T.P. Mommsen, and P.A. Wright. 1989. Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature 337:165-166.
95. 3H] nitroarginine into rat brain synaptosomes. J Neurochem 68:337-343.
96. Ratha B.K., N. Saha, R.K. Rana, and B. Chaudhury. 1995. Evolutionary significance of metabolic detoxification of ammonia to urea in an ammoniotelic freshwater teleost, Heteropneustes fossilis, during temporary water deprivation. Evol Biol (Bogota) 8/9:107-117.
97. Ritter N.M., D.D. Smith, Jr., and J.W. Campbell. 1987. Glutamine synthetase in liver and brain tissues of the holocephalan Hydrolagus colliei. J Exp Zool 243:181-188.
98. Rose C. 2002. Increased extracellular brain glutamate in acute liver failure: decreased uptake or increased release? Metab Brain Dis 17:251-261.
99. Rose C., A. Michalak, K.V. Rama Rao, G. Quack, G. Kircheis, and R.F. Butterworth. 1999. L-Ornithine-L-aspartate lowers plasma and cerebrospinal fluid ammonia and prevents brain edema in rats with acute liver failure. Hepatology 30:636-640.
100. Rozemeijer M.J.C. and I. Flaut. 1993. Regulation of nitrogen excretion of the amphibious blenniidae Alticus kirki (Guenther, 1868) during emersion and immersion. Comp Biochem Physiol A 104:57-62.
101. Saha N., L. Das, and S. Dutta. 1999. Types of carbamyl phosphate synthetases and subcellular localization of urea cycle and related enzymes in air-breathing walking catfish, Clarias batrachus, infused with ammonium chloride: a strategy to adapt under hyperammonia stress. J Exp Zool 283:121-130.
102. Saha N., L. Das, S. Dutta, and U.C. Goswami. 2001. Role of ureogenesis in the mud-dwelled Singhi catfish (Heteropneustes fossilis) under condition of water shortage. Comp Biochem Physiol A 128:137-146.
103. Saha N., J. Dkhar, P.M. Anderson, and B.K. Ratha. 1997. Carbamyl phosphate synthetase in an air-breathing teleost, Heteropneustes fossilis. Comp Biochem Physiol B 116:57-63.
104. Saha N. and B.K. Ratha. 1987. Active ureogenesis in a freshwater air-breathing teleost, Heteropneustes fossilis. J Exp Zool 241:137-141.
105. _. 1989. Comparative study of ureogenesis in freshwater air-breathing teleosts. J Exp Zool 252:1-8.
106. _. 1994. Induction of ornithine-urea cycle in a freshwater teleost, Heteropneustes fossilis, exposed to high concentrations of ammonium chloride. Comp Biochem Physiol 108B:315-325.
107. Sayer M.D.J. and J. Davenport. 1991. Amphibious fish: why do they leave water? Rev Fish Biol Fish 1:159-181.
108. Smart G.R. 1978. Investigations of the toxic mechanisms of ammonia to fish-gas exchange in rainbow trout (Salmo gairdneri) exposed to acutely lethal concentrations. J Fish Biol 12:93-104.
109. Smith D.D., Jr., N.M. Ritter, and J.W. Campbell. 1987. Glutamine synthetase isozymes in elasmobranch brain and liver tissues. J Biol Chem 262:198-202.
110. Sugden P.H. and E.A. Newsholme. 1975. The effects of ammonium, inorganic phosphate and potassium ions on the activity of phosphofructokinases from muscle and nervous tissues of vertebrates and invertebrates. Biochem J 150:113-122.
111. Szatkowski M., B. Barbour, and D. Attwell. 1990. Nonvesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 384:443-446.
112. Takahashi H., R.C. Koehler, S.W. Brusilow, and R.J. Traystman. 1991. Inhibition of brain glutamine accumulation prevents cerebral edema in hyperammonemic rats. Am J Physiol 261:H825-H829.
113. Tay S.L.A., S.F. Chew, and Y.K. Ip. 2003. The swamp eel Monopterus albus reduces endogenous ammonia production and detoxifies ammonia to glutamine during aerial exposure. J Exp Biol 206:2473-2486.
114. Tsui T.K.N., D.J. Randall, S.F. Chew, Y. Ji, J.M. Wilson, and Y.K. Ip. 2002. Accumulation of ammonia in the body and NH3 volatilization from alkaline regions of the body surface during ammonia loading and exposure to air in the weather loach Misgurnus anguillicaudatus. J Exp Biol 205:651-659.
115. Van den Thillart G. and M. van Raaij. 1995. Endogenous fuels: noninvasive versus invasive. Pp. 33-63 in P.W. Hochachka and T.P. Mommsen, eds. Biochemistry and Molecular Biology of Fishes. Vol. 4. Metabolic Biochemistry. Elsevier, Amsterdam.
116. van Waarde A. 1981. Nitrogen metabolism in goldfish Carassius aruatus (L.): activities of transamination reaction, purine nucleotide cycle and glutamate dehydrogenase in goldfish tissues. Comp Biochem Physiol B 68:407-413.
117. Vesce S., P. Bezzi, and A. Volterra. 2001. Synaptic transmission with glia. News Physiol Sci 16:178-184.
118. Walsh P.J., G.D. Mayer, M. Medina, M.L. Bernstein, J.F. Barimo, and T.P. Mommsen. 2003. A second glutamine synthetase gene with expression in the gills of the Gulf toadfish (Opsanus beta). J Exp Biol 206:1523-1533.
119. Walton M.J. and C.B. Cowey. 1977. Aspects of ammoniagenesis in rainbow trout, Salmo gairdneri. Comp Biochem Physiol 57:143-149.
120. Wilkie M.P. 1997. Mechanisms of ammonia excretion across fish gills. Comp Biochem Physiol 118:39-50.
121. Willard-Mack C.L., R.C. Koehler, T. Hirata, L.C. Cork, H. Takahashi, R.J. Traystman, and S.W. Brusilow. 1996. Inhibition of glutamine synthetase reduces ammonia-induced astrocyte swelling in rat. Neuroscience 71:589-599.
122. Wilson J.M., D.J. Randall, M. Donowitz, W.A. Vogl, and Y.K. Ip. 2000. Immunolocalization of ion transport proteins to the mudskipper (Periophthalmodon schlosseri) branchial epithelium mitochondria-rich cells. J Exp Biol 203:2297-2310.
123. Wilson J.M., D.J. Randall, T.W.K. Kok, W.A. Vogl, and Y.K. Ip. 1999. Fine structure of the gill epithelium of the terrestrial mudskipper, Periophthalmodon schlosseri. Cell Tissue Res 298:345-356.
124. Yokobori S., M. Hasegawa, T. Ueda, N. Okada, K. Nishikawa, and K. Watanabe. 1994. Relationship among coelacanths, lungfishes, and tetrapods: a phylogenetic analysis based on mitochondrial cytochrome oxidase I gene sequences. J Mol Evol 38:602-609.